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Buffalo liver transcriptome analysis suggests immune tolerance as its key adaptive mechanism during early postpartum negative energy balance

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Abstract

Females undergo negative energy balance (NEB) during the early postpartum period to meet the lactation demands. The liver, being the key metabolic organ, plays a major role in handling NEB. Dairy animals handling high lactation demands are better models to understand the liver adaptive mechanisms during this phase. Therefore, we analyzed the liver transcriptome of dairy buffaloes during early postpartum. Liver biopsies were performed on three lactating buffaloes on the 15th and the 30th days of early postpartum and three heifers (controls) at the diestrous stage. Paired-end Next Generation Sequencing (NGS) identified 509 significantly differentially expressed genes (SDE) in the liver among the three groups. The SDE with log2 fold change > 3 and the unique SDE revealed the promotion of immune suppression (e.g., TCR), apoptosis (e.g., CCDC103), PGF2α synthesis, fat accumulation (e.g., BGLAP) and liver regeneration (e.g., FGF10) pathways, and the downregulation of antigen presentation (e.g., BOLA-DQA) on the 15th day of lactation. Consistently upregulated genes on the 15th and 30th days of early postpartum indicated the promotion of immune tolerance (e.g., IFITM3), medium and long-chain fatty acids’ oxidation (e.g., ACSM3), and lipid accumulation (e.g., INSIG1). However, consistently downregulated genes during early postpartum showed immunosuppression, the downregulation of gluconeogenesis from amino acids (e.g., DDO), and the biosynthesis of taurine (e.g., CSAD) and unsaturated fatty acids (e.g., SCD). Functional annotation and network analyses also indicated the promotion of immune tolerance, fat accumulation and decreased gluconeogenesis from amino acids, and estrogen metabolism on the 15th day of lactation. Overall, the liver showed immune tolerance as an adaptive mechanism during early postpartum of buffaloes.

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Abbreviations

NEB:

Negative energy balance

NGS:

Next generation sequencing

BOLA-DQA :

Major histocompatibility complex, class II, DQ alpha, type 1

CCDC103 :

Coiled-coil domain-containing 103

PGF2α :

Prostaglandin F2alpha

BGLAP :

Bone gamma-carboxyglutamate

FGF10 :

Fibroblast growth factor 10

IFITM3 :

Interferon-induced transmembrane protein member 3

INSIG1 :

Insulin-induced gene 1

ACSM3 :

Acyl-CoA synthetase medium-chain family member 3

DDO :

D-aspartate oxidase

CSAD :

Cysteine sulfinic acid decarboxylase

SCD :

Stearoyl-CoA desaturase

ANGPTL4 :

Angiopoietin like 4

NEFA:

Non-esterified free fatty acids

FFA:

Free fatty acids

MAMPS:

Microbial associated molecular patterns

KEGG:

Kyoto encyclopaedia of gene and genome

GO:

Gene ontology

NCBI:

National Center for Biotechnology Information

STRING:

Search Tool for the Retrieval of Interacting Genes

PPI:

Protein- Protein interaction

FPKM:

Fragments per kilo-base of exon per million fragments mapped

GIMAP4 :

GTPase IMAP family member 4

BOLA-DQA5 :

Major histocompatibility complex, class II, DQ alpha, type 5

BOLA-DQB :

Major histocompatibility complex, class II, DQ alpha beta

USH1C :

USH1 Protein network component harmonin

M-SAA3.2 :

Mammary serum amyloid A3.2

SAA3 :

Serum amyloid A3

SLC22A16:

Solute carrier family 16

GSTA1:

Glutathione S-transferase A1

ECEL1 :

Endothelin-converting enzyme-like 1

PPAR:

Peroxisome proliferator-activated receptors

DQA2 :

Major histocompatibility complex, class II, DQ alpha 2

APOA1 :

Apolipoprotein A1

APOA5 :

Apolipoprotein A5

UBC :

Ubiquitin C

SECTM1A :

Secreted and transmembrane protein 1A

SH2D1A :

SH2 domain-containing 1A

LOC789452 :

T cell receptor alpha chain V region 2b4-like

PTGES :

Prostaglandin E synthase

LOC617406 :

Serpin peptidase inhibitor, clade B (ovalbumin), member 6-like

ncRNA:

Noncoding RNA

LOC100296286 :

T cell receptor alpha chain V region RL-5-like

LOC100300282 :

T cell receptor beta chain V region CTL-L17-like

IFI27L2 :

Interferon, alpha-inducible protein 27-like 2

HRAS :

HRas proto-oncogene, GTPase

GEFR :

Guanine nucleotide exchange factor

P2Y :

Purinergic receptor 2Y

LOC100848101 :

Kinesin-like protein KIF13A

TRNAR-CCG :

Transfer RNA arginine (anticodon CCG)

LOC615055 :

Ef-hand calcium-binding domain-containing protein 4A

LOC788915 :

Caspase-14

LOC107131362 :

UDP-Glucuronosyltransferase 2B33-like

SERPINE2 :

Serpin family E member 2

TPGS1 :

Tubulin polyglutamylase complex subunit 1

ASIP :

Agouti signaling protein

LOC101902932 :

Uncharacterized LOC101902932

C8G :

Complement component 8, gamma protein

ASPG :

Asparaginase

SPON2 :

Spondin 2

LOC785540 :

Cytochrome P450 2C31

LOC107133155 :

Apolipoprotein C-III-like

C4A :

Complement component 4A

LOC100337213 :

Adhesion G protein-coupled receptor E2

MT2A :

Metallothionein 2A

MT1E :

Metallothionein 1E

APOL3 :

Apolipoprotein L, 3

ABCA9 :

ATP binding cassette subfamily A member 9

GDPD1 :

Glycerophosphodiester phosphodiesterase domain-containing 1

DEPDC5 :

DEP domain-containing 5

MINOS1 :

Mitochondrial inner membrane organizing system 1

S1PR1 :

Sphingosine-1-phosphate receptor 1

PIK3CD :

Phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit delta

IGFBP1 :

Insulin-like growth factor binding protein 1

LOC511161 :

Nicotinamide N-methyltransferase

NKIRAS2 :

NF-KB inhibitor interacting Ras like2

LURAP1L:

Leucine rich adaptor protein 1 like

SPTCL3:

Serine palmitoyltransferase long-chain base subunit 3

KLF10 :

Kruppel like factor 10

LOC536097 :

Tyrosine-protein phosphatase non-receptor type substrate 1

ACTA2 :

Actin, alpha 2, smooth muscle, aorta

MTHFD1L :

Methylenetetrahydrofolate dehydrogenase 1-like

OAS1 :

2′,5′-oligoadenylate synthetase 1

OAS2 :

2′,5′-oligoadenylate synthetase 2

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Acknowledgments

The authors thank the Director, ICAR-National Dairy Research Institute and National Agricultural Science Fund, India, for providing the infrastructure and financial assistance (Grant No. NASF/GTR-5005/2015-16), respectively, to this work. Thanks to Mr. Ashwani Kumar, Director of NXGenbio Life Sciences for custom NGS analysis and Dr. Mamta Pandey for editing the tables and figures. The authors do not have any conflict of research and financial interests.

Funding

The National Agricultural Science Fund, India, provided the financial support to this work (Grant No. NASF/GTR-5005/2015–16).

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Authors and Affiliations

  1. Molecular Endocrinology, Functional Genomics and Systems Biology lab, Animal Biochemistry Division, ICAR-National Dairy Research Institute, Karnal, 132001, India

    Sudhakar Singh, Naresh Golla, Davinder Sharma, Dheer Singh & Suneel Kumar Onteru

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  1. Sudhakar Singh
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  2. Naresh Golla
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  3. Davinder Sharma
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Contributions

SKO and DS designed and organized the research work. SS, NG, and DaS performed experiments. SS and SKO analyzed the data. SS, DS, and SKO wrote the manuscript.

Corresponding author

Correspondence to Suneel Kumar Onteru.

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A total of six healthy buffaloes considered in the present study were approved by the Institutional Animal Ethics Committee of the National Dairy Research Institute, Karnal (Approval no. 95/16).

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The authors declare that they have no conflict of interests.

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Singh, S., Golla, N., Sharma, D. et al. Buffalo liver transcriptome analysis suggests immune tolerance as its key adaptive mechanism during early postpartum negative energy balance. Funct Integr Genomics 19, 759–773 (2019). https://doi.org/10.1007/s10142-019-00676-1

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